Rapid Hydrolysis of Quorum‐Sensing Molecules in the Gut of Lepidopteran Larvae

Funke, Matthias; Büchler, Rita; Mahobia, Vertica; Schneeberg, Alexander; Ramm, Michael; Boland, Wilhelm

doi:10.1002/cbic.200700781

Cited by 41 publications

(35 citation statements)

References 45 publications

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“…1C). Despite its simplicity, a large amount of bacteria, exceeding 10 7 mL −1 [22], has been found occupying the gut and a high concentration of nutritive glucose is liberated there, making the gut an ideal environment for diverse microbial activities, including fermentation. These properties make this organism an ideal naturally-occurring model in which to study digestive-tract microbial symbiosis.…”

Section: Discussionmentioning

confidence: 99%

“…The simplicity of this community, comprised of 22–42 OTUs, is especially apparent compared to the gut microbiota of insects from orders such as termites of Isoptera, or vertebrates, which often harbor hundreds of phylotypes [28], [29]. Strong alkalinity in the gut, considered an important determinant of community structure in beetle larvae, could also be the case in Spodoptera , which has a midgut pH >10 [22], [30]. Other key factors, including a fast food throughput and immune system function, may also account for this taxonomically restricted gutflora [31].…”

Section: Discussionmentioning

confidence: 99%

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In Vivo Pyro-SIP Assessing Active Gut Microbiota of the Cotton Leafworm, Spodoptera littoralis

Shao

Arias-Cordero²,

Guo³

et al. 2014

PLoS ONE

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The gut microbiota is of crucial importance for the host with considerable metabolic activity. Although great efforts have been made toward characterizing microbial diversity, measuring components' metabolic activity surprisingly hasn't kept pace. Here we combined pyrosequencing of amplified 16S rRNA genes with in vivo stable isotope probing (Pyro-SIP) to unmask metabolically active bacteria in the gut of cotton leafworm (Spodoptera littoralis), a polyphagous insect herbivore that consumes large amounts of plant material in a short time, liberating abundant glucose in the alimentary canal as a most important carbon and energy source for both host and active gut bacteria. With 13C glucose as the trophic link, Pyro-SIP revealed that a relatively simple but distinctive gut microbiota co-developed with the host, both metabolic activity and composition shifting throughout larval stages. Pantoea, Citrobacter and Clostridium were particularly active in early-instar, likely the core functional populations linked to nutritional upgrading. Enterococcus was the single predominant genus in the community, and it was essentially stable and metabolically active in the larval lifespan. Based on that Enterococci formed biofilm-like layers on the gut epithelium and that the isolated strains showed antimicrobial properties, Enterococcus may be able to establish a colonization resistance effect in the gut against potentially harmful microbes from outside. Not only does this establish the first in-depth inventory of the gut microbiota of a model organism from the mostly phytophagous Lepidoptera, but this pilot study shows that Pyro-SIP can rapidly gain insight into the gut microbiota's metabolic activity with high resolution and high precision.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

In Vivo Pyro-SIP Assessing Active Gut Microbiota of the Cotton Leafworm, Spodoptera littoralis

Shao

Arias-Cordero²,

Guo³

et al. 2014

PLoS ONE

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“…1). This apparently simple transformation could not be achieved in vitro and was not simply pH-dependent [pH of the Lepidopteran foregut is approximately 10.5 (13)], but required a hitherto unknown enzymatic activity, formally related to the transformation of prostaglandin A 1 to prostaglandin B 1 , which is known from several mammalian species ( Fig. 1) (14).…”

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confidence: 99%

The phytohormone precursor OPDA is isomerized in the insect gut by a single, specific glutathione transferase

Dąbrowska¹,

Freitak

Vogel

et al. 2009

Proc. Natl. Acad. Sci. U.S.A.

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Oxylipins play important roles in stress signaling in plants. The compound 12-oxophytodienoic acid (cis-OPDA) is an early biosynthetic precursor of jasmonic acid (JA), the key phytohormone orchestrating the plant anti-herbivore defense. When consumed by feeding Lepidopteran larvae, plant-derived cis-OPDA suffers rapid isomerization to iso-OPDA in the midgut and is excreted in the frass. Unlike OPDA epimerization (yielding trans-OPDA), the formation of iso-OPDA is enzyme-dependent, and is catalyzed by an inducible glutathione transferase (GSTs) from the larval gut. Purified GST fractions from the gut of Egyptian cotton leafworm (Spodoptera littoralis) and cotton bollworm (Helicoverpa armigera) both exhibited strong OPDA isomerization activity, most likely via transient formation of a glutathione-OPDA conjugate. Out of 16 cytosolic GST proteins cloned from the gut of cotton bollworm larvae and expressed in E. coli, only one catalyzed the OPDA isomerization. The biological function of the double bond shift might be seen in an inactivation of cis-OPDA, similar to the inactivation of prostaglandin A1 to prostaglandin B1 in mammalian tissue. The enzymatic isomerization is particularly widespread among generalist herbivores that have to cope with various amounts of cis-OPDA in their spectrum of host plants.12-oxophytodienoic acid ͉ inactivation of OPDA

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“…Furthermore, constant change in gut contents due to molting and metamorphosis can affect the colonization of microorganisms. Many insects have an intestinal pH in the range of 6-8, and some lepidopteran larvae have an even higher pH (11-12) in their midguts [124,125]. The hindgut harbors high bacterial diversity and density in several insects, such as cockroaches, crickets and termites [126][127][128].…”

Section: Discussionmentioning

confidence: 99%

The Microbiome of Spodoptera littoralis: Development, Control and Adaptation to the Insect Host

Mazumdar¹,

Teh²,

Boland³

2018

Metagenomics for Gut Microbes

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The symbiotic microbial consortium in the gut of Spodoptera littoralis shows dramatic, but reproducible changes in line with the development of the insect from the egg via six larval instars to the pupa. Since the food is kept constant during development, factors from the insect host and certain microbial symbionts are assumed to control the composition of the microbiome. A GFP-tagged Enterococcus mundtii, one of the major players of the consortium, easily integrates into the microbiome and can be monitored in all gut segments at all developmental stages. The reporter organism can be recovered from the gut using a preparative flow cytometry allowing subsequent RNA extraction for transcriptomic analyses. The transcriptomic profile from the fluorescent Enterococcus cells provides information on the adaptation of the reporter organism to the local gut conditions. The concept of using a fluorescent reporter organism that can be recovered at any time from any area of the intestinal tract will allow a holistic analysis of adaptation strategies used by the microbes to adapt to the insect gut. In combination with the analysis of transcript patterns from the gut membranes, a first insight into the molecular interaction between the insect host and the microbiome can be expected.

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Rapid Hydrolysis of Quorum‐Sensing Molecules in the Gut of Lepidopteran Larvae

Cited by 41 publications

References 45 publications

In Vivo Pyro-SIP Assessing Active Gut Microbiota of the Cotton Leafworm, Spodoptera littoralis

In Vivo Pyro-SIP Assessing Active Gut Microbiota of the Cotton Leafworm, Spodoptera littoralis

The phytohormone precursor OPDA is isomerized in the insect gut by a single, specific glutathione transferase

The Microbiome of Spodoptera littoralis: Development, Control and Adaptation to the Insect Host

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